Chromatin Remodeler TaSWI3D Controls Wheat Susceptibility to Pathogenic Fungus Blumeria graminis forma specialis tritici

Pathogenic fungus Blumeria graminisforma specialistritici (B.g. tritici) is the causal agent of the devastating wheat powdery mildew disease. Identifying the key regulators governing wheat susceptibility to the B.g. tritici pathogen is essential for developing wheat varieties with improved powdery mildew resistance. In this study, we demonstrated that the wheat chromatin remodeler TaSWI3D positively regulates wheat susceptibility to B.g. tritici. Overexpression of TaSWI3D gene attenuates wheat resistance against B.g. tritici, while silencing of TaSWI3D gene potentiates wheat powdery mildew resistance. TaSWI3D protein was found to be enriched at the promoter regions of the TaSARD1 gene encoding the salicylic acid (SA) biosynthesis activator, and silencing of TaSWI3D resulted in decreased nucleosome occupancy at the TaSARD1 promoter regions. Activated TaSARD1 transcription and increased SA accumulation were observed in the TaSWI3D-silenced wheat plants. Silencing of TaSARD1 and the SA biosynthesis gene TaICS1 resulted in attenuated SA biosynthesis and decreased powdery mildew resistance in the TaSWI3D-silenced wheat plants. These findings support that the chromatin remodeler TaSWI3D maintains epigenetic suppression of the SA biosynthesis activator gene TaSARD1 and negatively regulates SA biosynthesis, thereby positively contributing to wheat powdery mildew susceptibility.